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An evolutionarily distinct family of polysaccharide lyases removes rhamnose capping of complex arabinogalactan proteins

Abstract : The human gut microbiota utilizes complex carbohydrates as major nutrients. The requirement for efficient glycan degrading systems exerts a major selection pressure on this microbial community. Thus, we propose that this microbial ecosystem represents a substantial resource for discovering novel carbohydrate active enzymes. To test this hypothesis we screened the potential enzymatic functions of hypothetical proteins encoded by genes of Bacteroides thetaiotaomicron that were up-regulated by arabinogalactan proteins or AGPs. Although AGPs are ubiquitous in plants, there is a paucity of information on their detailed structure, the function of these glycans in planta, and the mechanisms by which they are depolymerized in microbial ecosystems. Here we have discovered a new polysaccharide lyase family that is specific for the L-rhamnose-alpha 1,4-D-glucuronic acid linkage that caps the side chains of complex AGPs. The reaction product generated by the lyase, Delta 4,5-unsaturated uronic acid, is removed from AGP by a glycoside hydrolase located in family GH105, producing the final product 4-deoxy-beta-L-threo-hex-4-enepyranosyl- uronic acid. The crystal structure of a member of the novel lyase family revealed a catalytic domain that displays an (alpha/alpha)(6) barrel-fold. In the center of the barrel is a deep pocket, which, based on mutagenesis data and amino acid conservation, comprises the active site of the lyase. A tyrosine is the proposed catalytic base in the beta-elimination reaction. This study illustrates how highly complex glycans can be used as a scaffold to discover new enzyme families within microbial ecosystems where carbohydrate metabolism is a major evolutionary driver.
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Jose Munoz-Munoz, Alan Cartmell, Nicolas Terrapon, Arnaud Basle, Bernard Henrissat, et al.. An evolutionarily distinct family of polysaccharide lyases removes rhamnose capping of complex arabinogalactan proteins. Journal of Biological Chemistry, American Society for Biochemistry and Molecular Biology, 2017, 292 (32), pp.13271 - 13283. ⟨10.1074/jbc.M117.794578⟩. ⟨hal-01606932⟩

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